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Dantzer, B.

Publications and source records attributed to Dantzer, B..

At least 19 recordsLinked to original sources

Maternal effects shape scale-dependent convergence in gut microbial responses to environmental change

Animals can experience environmental variability across multiple temporal scales, from predictable within-year seasonal fluctuations to rarer, irregular resource pulses that occur across generations. While gut microbiome responses to seasonal changes are well documented, far less is understood about how host-associated microbiomes respond to episodic environmental resource pulses, and whether such responses can persist across generations. Here, we investigate how gut microbial communities of wild North American red squirrels (Tamiasciurus hudsonicus) respond to intra-annual seasonal variation and episodic resource pulses happening years apart (specifically, seed masting). We then test the hypothesis that these responses are shared by mothers and their offspring. In line with prior work across mammals, we found that seasonal variation strongly structured gut microbiomes, driving widespread and convergent shifts in composition across the year. However, episodic resource pulses predicted microbial scatter such that gut microbiomes became more dissimilar across individuals in resource pulse years compared to typical years. Despite this population-level divergence, mothers and their adult offspring exhibited microbial convergence when encountering resource pulses occurring years apart, whereas seasonal responses were shared across the population and not unique to mother-offspring pairs. Overall, our results highlight the mammalian gut microbiome as a flexible component of the host phenotype, capable of adjusting to both predictable seasonal variation and large-scale, episodic resource pulses. Patterns of mother-offspring similarity across resource pulse years further provide evidence that some host-microbial responses to environmental change may be transmitted across generations.

ecology↗

Developmental conditions shape lifetime reproductive strategies in a wild mammal

Coping with developmental hardship is a defining feature of resilience across the tree of life. Compensatory strategies that preserve fitness after a poor start are hypothesized to be favored by natural selection, but empirical evidence is rare. Using over three decades of data on >1,000 reproductive attempts across the lifetimes of 405 wild female red squirrels, we show that developmental adversity prompts adaptive reorganization of reproductive investment across the lifespan. Hardships reduced lifetime reproductive opportunities, but triggered opposing strategies. Extrinsic mortality risk predicted frontloading of reproduction at debut, while poor maternal investment predicted terminal reproductive effort at a cost to future generations. Both strategies preserved lifetime fitness, revealing how context-dependent reproductive plasticity over the life course can rescue the fitness consequences of developmental hardship.

ecology↗

Territorial behavior as a route of social microbial transmission in an asocial mammal

Microbial transmission is a major benefit of sociality, facilitated by affiliative behaviors such as grooming and communal nesting in group-living animals. The spread of microbial symbionts through these pathways, and their incorporation into host microbiomes, can enhance host health and fitness by contributing to pathogen protection and metabolic flexibility. Are pathways that facilitate microbial transfer across hosts also present in animals that do not form social groups because territoriality limits social interactions and prevents group formation? Here, we addressed this question by combining longitudinal sampling of individual gut microbial communities, demographic data, and dynamic behavioral and spatial measures of territoriality from a non-social, highly territorial small mammal: wild North American red squirrels (Tamiasciurus hudsonicus). As squirrel densities increased, individual gut microbial communities became richer and more phylogenetically diverse, while among-individual differences in composition decreased. This pattern was characterized primarily by increases in obligately anaerobic and non-sporulating taxa with little to no tolerance for oxygen-rich environments, suggesting social rather than environmental routes of transmission. Moreover, territorial intrusions--in which conspecifics were found on within an individuals territorial space--increased gut microbial diversity among individuals defending larger territorial spaces. Using an intrusion-based social network analysis, we found that that pairs with stronger social association (via intrusions) exhibited higher gut microbial similarity. Taken together, our findings provide some of the first evidence for social microbial transmission in a non-social species, and suggest that increased density and territorial behavior can diversify and homogenize host gut microbial communities despite social isolation.

ecology↗

Timing-dependent effects of elevated maternal glucocorticoids on offspring brain gene expression in a wild small mammal

An increase in maternal stress during offspring development can have cascading, life-long impacts on offspring behavior and physiology, which can vary depending on the timing of exposure to the stressor. By responding to stressors through increasing production of glucocorticoids (GCs), the hypothalamic-pituitary-adrenal (HPA) axis is a key mediator of maternal effects - both on the side of the mother and the offspring. At a molecular level, maternal effects are thought to be mediated through modifying transcription of genes, particularly in the brain. To better understand the evolutionary implications of maternal effects, more studies are needed on mechanisms of maternal effects in wild populations. To test how the timing of maternal stress impacts gene expression in the brains of offspring, we treated free-ranging North American red squirrels (Tamiasciurus hudsonicus) with GCs during late pregnancy or early lactation and collected brains from offspring around weaning. We used RNA-sequencing to measure gene expression in the hypothalamus and hippocampus. We found small differences in gene expression between GC-treated and control individuals suggesting long-term effects of the GC treatment on neural gene transcription. The general patterns of gene regulation across the transcriptome were consistent between the pregnancy and lactation-treated individuals. However, the number of significantly differentially expressed genes was higher in the lactation treatment group. These results support the idea that maternal stress affects neural gene expression in offspring, and these effects are dependent on timing. Our findings add valuable insight into the impact of maternal hormones on neural transcriptomics in a wild population.

ecology↗

A Wireless Wearable Ecosystem for Social Network Analysis in Free-living Animals

Understanding the dynamics of animal social systems requires studying variation in contact and interaction, which is influenced by environmental conditions, resource availability, and predation risk, among other factors. Traditional (direct) observational methods have limitations, but advancements in sensor technologies and data analytics provide unprecedented opportunities to study these complex systems in naturalistic environments. Proximity logging and tracking devices, capturing movement, temperature, and social interactions, offer non-invasive means to quantify behavior and develop empirical models of animal social networks. However, challenges remain in integrating different data types, incorporating more sensor modalities, and addressing logistical constraints. To address these gaps, we developed a wireless wearable sensor system with novel features (called "Juxta"), including modular battery packs, memory management for combining data types, reconfigurable deployment modes, and a smartphone app for data collection. We present data from a pilot study on prairie voles (Microtus ochrogaster), which is a small mammal species that exhibits relatively complex social behavior. We demonstrate the potential for Juxta to increase our understanding of the social networks and behavior of free-living animals. Additionally, we propose a framework to guide future research in merging temporal, spatial, and event-driven data. By leveraging wireless technology, battery efficiency, and smart sensing modalities, our wearable ecosystem offers a scalable solution for real-time, high-resolution data capture and analysis in animal social network studies, opening new avenues for exploring complex social dynamics across species and environments.

animal behavior and cognition↗

A future food boom rescues the negative effects of cumulative early-life adversity on lifespan in a small mammal

Adverse early-life conditions, even when transient, can have long-lasting effects on individual phenotypes and reduce lifespan across species. If these effects can be mitigated. by a high quality later-life environment, then differences in future resource access may explain variation in vulnerability and resilience to early-life adversity. Using 32 years of data on 1,000+ wild North American red squirrels, we tested the hypothesis that the negative effects of early-life adversity on lifespan can be buffered by later-life food abundance. We found that although cumulative early-life adversity was negatively associated with adult lifespan, this relationship was modified by future food abundance. Squirrels that experienced a naturally-occurring future food boom in the second year of life did not suffer reduced longevity despite early-life adversity. Experimental supplementation with additional food did not replicate this effect, though it did increase adult lifespan overall. Our results suggest a non-deterministic role for early-life conditions on later-life phenotypes, and highlight the importance of contextualizing the influence of harsh early-life conditions over an animals entire life course.

evolutionary biology↗

Interpretation of body condition index should be informed by natural history

Many studies assume that it is beneficial for individuals of a species to be heavier, or have a higher body condition index (BCI), without accounting for the physiological relevance of variation in the composition of different body tissues. We hypothesized that the relationship between BCI and masses of physiologically important tissues (fat and lean) would be conditional on annual patterns of energy acquisition and expenditure. We studied three species with contrasting ecologies in their respective natural ranges: an obligate hibernator (Columbian ground squirrel, Urocitellus columbianus), a facultative hibernator (black-tailed prairie dog, Cynomys ludovicianus), and a food-caching non-hibernator (North American red squirrel, Tamiasciurus hudsonicus). We measured fat and lean mass in adults of both sexes using quantitative magnetic resonance (QMR). We measured body mass and two measures of skeletal structure (zygomatic width and right hind foot length) to develop sex- and species-specific BCIs, and tested the utility of BCI to predict body composition in each species. Body condition indices were more consistently, and more strongly correlated, with lean mass than fat mass. The indices were most positively correlated with fat when fat was expected to be very high (pre-hibernation prairie dogs). In all cases, however, BCI was never better than body mass alone in predicting fat or lean mass. While the accuracy of BCI in estimating fat varied across the natural histories and annual energetic patterns of the species considered, measuring body mass alone was as effective, or superior in capturing sufficient variation in fat and lean in most cases.

physiology↗

Benefits of living closer to kin vary by genealogical relationship in a territorial mammal

While cooperative interactions among kin are a key building block in the societies of group-living species, their importance for species with more variable social environments is unclear. North American red squirrels (Tamiasciurus hudsonicus) defend individual territories in dynamic neighbourhoods and are known to benefit from living among familiar conspecifics, but not relatives. However, kin-directed behaviours may be restricted to specific genealogical relationships or strongly mediated by geographic distance, masking their influence at broader scales. Using distance between territories as a proxy for the ability of individuals to interact, we estimated the influence of primary kin (parents, offspring, siblings) on the annual survival and reproductive success of red squirrels. This approach revealed associations between fitness and access to kin, but only for certain genealogical relationships and fitness components. For example, females had enhanced annual survival when living closer to their daughters, though the reverse was not true. Most surprising was the finding that males had higher annual reproductive success when living closer to their father, suggesting possible recognition and cooperation among fathers and sons. Together, these findings point to unexpected nuance in the fitness consequences of kinship dynamics for a species that is territorial and largely solitary.

animal behavior and cognition↗

Using a Homeogram to Detect Sleep in Free-living Animals

O_LISleep is appreciated as a behavior critical to homeostasis, performance, and fitness. Yet, most of what we know about sleep comes from humans or controlled laboratory experiments. Assessing sleep in wild animals is challenging, as it is often hidden from view, and electrophysiological recordings that define sleep states are difficult to obtain. Accelerometers have offered great insight regarding gross movement, although ambiguous quiescent states like sleep have been largely ignored, limiting our understanding of this ubiquitous behavior. C_LIO_LIWe developed a broadly applicable sleep detection method called a homeogram that can be applied to accelerometer data collected from wild animals. We applied our methodology to detect sleep in free-ranging North American red squirrels (Tamiasciurus hudsonicus) in a region that experiences drastic seasonal shifts in light, temperature, and behavioral demands. C_LIO_LIOur method characterized sleep in a manner consistent with limited existing studies and expanded those observations to provide evidence that red squirrels apply unique sleep strategies to cope with changing environments. C_LIO_LIApplying our analytical strategy to accelerometer data from other species may open new possibilities to investigate sleep patterns for researchers studying wild animals. C_LI

animal behavior and cognition↗

Urban fox squirrels exhibit habituation to humans but respond to stimuli from natural predators

Animals in urban areas that experience frequent exposure to humans often behave differently than those in less urban areas, such as exhibiting less vigilance or anti-predator behavior. These behavioral shifts may be an adaptive response to urbanization, but it may be costly if animals in urban areas also exhibit reduced anti-predator behavior in the presence of natural predators. In trials with only a human observer as the stimulus, urban squirrels exhibited reduced vigilance and anti-predator behavior compared to those in less urban areas. Next, we exposed squirrels in multiple urban and less urban sites to acoustic playbacks of a control stimulus (non-predatory bird calls), a natural predator (hawk), and dogs and recorded their vigilance and three different anti-predator behaviors when a human approached them while either broadcasting one of these three playbacks or no playbacks at all. Squirrels at urban sites also did not differ in their behavioral responses to the playbacks from possible predators (hawks or dogs) when they were compared to those at less urban sites exposed to these playbacks. Urban squirrels also exhibited increased vigilance and anti-predator behavior when exposed to a human paired with hawk playbacks compared to the control playbacks. Together, our results indicate that urban squirrels did perceive and assess risk to the natural predator appropriately despite exhibiting increased tolerance to humans. These results provide little support for the hypothesis that increased tolerance to humans causes animals to lose their fear of natural predators.

animal behavior and cognition↗

Maternal glucocorticoids do not influence HPA axis activity or behavior of juvenile wild North American red squirrels

Environmental factors experienced during development can affect the physiology and behavior of offspring. Maternal glucocorticoids (GCs) may convert environmental cues experienced by the mother into a cue triggering adaptive developmental plasticity in offspring. In North American red squirrels (Tamiasciurus hudsonicus), females exhibit increases in GCs when conspecific density is elevated, and selection favors more aggressive and perhaps more active mothers under high density conditions. We experimentally elevated maternal GCs during gestation or early lactation to test the hypothesis that elevated maternal GCs cause shifts in offspring aggression and activity that may prepare them for high density conditions. When offspring were weaned, we measured two behavioral traits (activity and aggression) using a standardized behavioral assay. Because maternal GCs may influence offspring hypothalamic-pituitary-adrenal (HPA) axis activity and HPA axis activity may in turn affect offspring behavior, we also measured the impact of our treatments on offspring HPA axis activity (adrenal reactivity and negative feedback) and the association between offspring HPA axis activity and behavior. Increased maternal GCs during lactation, but not gestation, only slightly elevated activity levels in offspring. Offspring aggression, adrenal reactivity, and negative feedback did not differ between GC-treated and control groups. Offspring with higher adrenal reactivity did exhibit lower aggression, but the relationship between adrenal reactivity and aggression was not affected by treatment with maternal GCs. These results suggest maternal GCs during gestation or early lactation alone may not be a sufficient cue to produce changes in behavioral and physiological stress responses in offspring in natural populations. Summary StatementWe found maternal glucocorticoid levels do not influence offspring personality or HPA axis dynamics in North American red squirrels. Regardless of maternal glucocorticoid treatment, more aggressive squirrels exhibited lower adrenal reactivity.

animal behavior and cognition↗

Maternal stress promotes offspring growth without oxidative costs in wild red squirrels

Elevations in glucocorticoid levels (GCs) in breeding females may induce adaptive shifts in offspring life histories. Offspring produced by mothers with elevated GCs may be better prepared to face harsh environments where a faster pace of life is beneficial. We examined how experimentally elevated GCs in pregnant or lactating North American red squirrels (Tamiasciurus hudsonicus) affected offspring postnatal growth, structural size, oxidative stress levels (two antioxidants and oxidative protein damage) in three different tissues (blood, heart, liver), and liver telomere lengths. We predicted that offspring from mothers treated with GCs would grow faster but would also have higher levels of oxidative stress and shorter telomeres, which may predict reduced longevity. Offspring from mothers treated with GCs during pregnancy were 8.3% lighter around birth but grew (in body mass) 17.0% faster than those from controls, whereas offspring from mothers treated with GCs during lactation grew 34.8% slower than those from controls and did not differ in body mass around birth. Treating mothers with GCs during pregnancy or lactation did not alter the oxidative stress levels or telomere lengths of their offspring. Fast-growing offspring from any of the treatment groups did not have higher oxidative stress levels or shorter telomere lengths, indicating that offspring that grew faster early in life did not exhibit oxidative costs after this period of growth. Our results indicate that elevations in maternal GCs may induce plasticity in offspring growth without long-term oxidative costs to the offspring that might result in a shortened lifespan. Summary StatementWe show that experimental increases in glucocorticoids in breeding female North American red squirrels affects offspring postnatal growth but not levels of oxidative damage and antioxidants or telomere lengths.

evolutionary biology↗

How does individual variation in sociality influence fitness in prairie voles?

Comparative studies aid in our understanding of specific conditions favoring the initial evolution of different types of social behaviors, yet there is much unexplained intraspecific variation in the expression of social behavior that comparative studies have not yet addressed. The proximate causes of this individual variation in social behavior within a species have been examined in some species but its fitness consequences have been less frequently investigated. In this study, we quantified the fitness consequences of variation in the sociality of prairie voles (Microtus ochrogaster). We characterized sociality of voles in semi-natural enclosures using an automated behavioral tracking system paired with social network analyses to quantify the degree of spatial and temporal co-occurrence of different voles. We then assessed the relationship between sociality with mating success (number of different conspecifics with which an individual produced offspring) and reproductive success (total number of offspring surviving to first capture). We measured the number of social connections each individual had with all voles and only with opposite-sex voles by calculating unweighted degree through social network analyses. Both female and male voles varied in the number of social connections they had with all conspecifics and with opposite-sex conspecifics. Voles with an intermediate number of social connections with voles of both sexes had higher mating success overall. In our analyses that considered all social connections with voles of both sexes, voles with an intermediate number of social connections produced more offspring. Males with a very high or low number of social connections also had the lowest average body mass. Overall, our results suggest some limit on the fitness benefits of sociality. Although there was substantial individual-variation in our measure of vole social behavior, intermediate levels of social connections may be most favorable.

animal behavior and cognition↗

Museum epigenomics: characterizing cytosine methylation in historic museum specimens

Museum genomics has transformed the field of collections-based research, opening up a range of new research directions for paleontological specimens as well as natural history specimens collected over the past few centuries. Recent work demonstrates that it is possible to characterize epigenetic markers such as DNA methylation in well-preserved ancient tissues. This approach has not yet been tested in traditionally-prepared natural history specimens such as dried bones and skins, the most common specimen types in vertebrate collections. In this study, we develop and test methods to characterize cytosine methylation in dried skulls up to 76 years old. Using a combination of ddRAD and bisulfite treatment, we characterized patterns of cytosine methylation in two species of deer mouse (Peromyscus spp.) collected in the same region in Michigan in 1940, 2003, and 2013-2016. We successfully estimated methylation in specimens of all age groups, though older specimens yielded less data and showed greater interindividual variation in data yield than newer specimens. Global methylation estimates were reduced in the oldest specimens (76 years old) relative to the newest specimens (1-3 years old), which may reflect post mortem hydrolytic deamination. Methylation was reduced in promoter regions relative to gene bodies and showed greater bimodality in autosomes relative to female X chromosomes, consistent with expectations for methylation in mammalian somatic cells. Our work demonstrates the utility of historic specimens for methylation analyses, as with genomic analyses; however, such studies will need to accommodate the large variance in the quantity of data produced by older specimens.

genomics↗

Individual variation in phenotypic plasticity of the stress axis

Phenotypic plasticity--one individuals capacity for phenotypic variation under different environments--is critical for organisms facing fluctuating conditions within their lifetime. North American red squirrels (Tamiasciurus hudsonicus) experience drastic among-year fluctuations in conspecific density. This shapes juvenile competition over vacant territories and overwinter survival. To help young cope with competition at high densities, mothers can increase offspring growth rates via a glucocorticoid-mediated maternal effect. However, this effect is only adaptive under high densities, and faster growth often comes at a cost to longevity. While experiments have demonstrated that red squirrels can adjust hormones in response to fluctuating density, the degree to which mothers differ in their ability to regulate glucocorticoids across changing densities remains unknown--little is known about within-individual plasticity in endocrine traits relative to among-individual variation. Findings from our reaction norm approach revealed significant individual variation not only in a female red squirrels mean endocrine phenotype, but also in endocrine plasticity in response to changes in local density. Future work on the proximate and ultimate drivers of variation in the plasticity of endocrine traits and maternal effects is needed, particularly in free-living animals experiencing fluctuating environments.

zoology↗

Territory acquisition mediates the influence of predators and climate on juvenile red squirrel survival

1) Juvenile survival to first breeding is a key life history stage. Survival through this period can be particularly challenging when it coincides with harsh environmental conditions like winter climate or food scarcity, and so cohort survival can be highly variable. However, the small size and dispersive nature of juveniles makes studying their survival difficult.\n2) In territorial species, a key life history event is the acquisition of a territory. A territory is expected to enhance survival, but how it does so, possibly through mediating mortality, is not often identified. We tested how the timing of territory acquisition influenced the survival of juvenile North American red squirrels Tamiasciurus hudsonicus, hereafter red squirrels, and how the timing of this event mediated sources of mortality. We hypothesized that securing a territory prior to the caching season would reduce juvenile susceptibility to predation or climatic factors over winter.\n3) Using 27 years of data on the survival of individually-marked juvenile red squirrels, we tested how the timing of territory acquisition influenced survival, whether the population density of red squirrel predators and mean temperature over winter were related to individual survival probability, and if territory ownership mediated these effects.\n4) Juvenile survival was lower in years of high predator abundance and in colder winters. Autumn territory owners were less susceptible to lynx Lynx canadensis, and possibly mustelid Mustela and Martes spp., predation. Autumn territory owners had lower survival in colder winters, while non-owners had higher survival in cold winters.\n5) Our results show how the timing of a life history event like territory acquisition can directly affect survival and also mediate the effects of biotic and abiotic factors later in life. This engenders a better understanding of the fitness consequences of the timing of key life history events.

ecology↗

Fitness benefits of a motivated mom

Parental investment theory predicts that observed levels of parental care afforded to offspring are set by the benefits (to offspring quality and survival) relative to the costs (to parental survival or future reproduction). Although difficult to document in mammals, there is often substantial individual-variation in the amount of parental care within species. We measured the impact of individual variation in maternal care (\"attentiveness\" towards offspring or maternal motivation) on offspring growth and survival in a wild population of North American red squirrels (Tamiasciurus hudsonicus). We used latency to return to pups following a nest intrusion as a measure of maternal attentiveness to pups. We found this behavior to be repeatable within individuals suggesting this behavior is a personality trait or a \"maternal style\". In this population, postnatal growth rate is important for pup overwinter survival. Pups from large litters grew faster if they had a highly attentive mother, indicating that maternal care behavior can mitigate the trade-off between litter size and offspring growth and potentially improve survival of pups. Additionally, more attentive mothers had slightly higher lifetime reproductive success than less attentive mothers. These results highlight important fitness effects of having a highly attentive mother and show that maternal care behavior can alter a fundamental life history trade-off between offspring quantity and quality.\n\nLay SummaryIt pays to be attentive to your pups as a squirrel mom. In a long-term study of a wild population of North American red squirrels, we observed repeatable individual variation in maternal attentiveness towards offspring. Mothers who returned faster to pups following a nest intrusion produced faster growing pups and were able to produce larger fast-growing litters. Over their entire lifetime, attentive mothers also had more offspring recruit into the breeding population.

evolutionary biology↗

Familiar neighbors, but not relatives, enhance fitness in a territorial mammal

SummaryOne of the outstanding questions in evolutionary biology is the extent to which mutually beneficial interactions and kin-selection can facilitate the evolution of cooperation by mitigating conflict between interacting organisms. The indirect fitness benefits gained from associating with kin are an important pathway to conflict resolution [1], but conflict can also be resolved if individuals gain direct benefits from cooperating with one another (e.g. mutualism or reciprocity) [2]. Owing to the kin-structured nature of many animal societies, it has been difficult for previous research to assess the relative importance of these mechanisms [3-5]. However, one area that might allow for the relative roles of kin-selection and mutualistic benefits to be disentangled is in the resolution of conflict over territorial space [6]. While much research has focused on group-living species, the question of how cooperation can first be favoured in solitary, territorial species remains a key question. Using 22 years of data from a population of North American red squirrels, we assessed how kinship and familiarity with neighbours affected fitness in a territorial mammal. While living near kin did not enhance fitness, familiarity with neighbours increased survival and annual reproductive success. These fitness benefits were strong enough to compensate for the effects of aging later in life, with potential consequences for the evolution of senescence. We suggest that such substantial fitness benefits provide the opportunity for the evolution of cooperation between adversarial neighbours, offering insight into the role that mutually beneficial behaviours might play in facilitating and stabilizing social systems. Graphical Abstract O_FIG_DISPLAY_L [Figure 1] M_FIG_DISPLAY C_FIG_DISPLAY

evolutionary biology↗